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Aquatic Sciences

, 81:60 | Cite as

Extreme rates and diel variability of planktonic respiration in a shallow sub-arctic lake

  • Matthew J. BogardEmail author
  • Sarah Ellen Johnston
  • Mark. M. Dornblaser
  • Robert G. M. Spencer
  • Robert G. Striegl
  • David E. Butman
Research Article

Abstract

Planktonic community respiration (CR) is a major component of aquatic biogeochemical cycling and food web energetics. Accurate, direct characterizations of short-term patterns and drivers of plankton CR are needed to understand aquatic biogeochemical processes and food web functioning. Recent work indicates CR may be commonly underestimated, and may undergo considerable diel changes that are missed using standard methodological approaches. To explore these possibilities, we applied an immediate, in situ, dark incubation approach at ~ 3 h intervals over 2.5 diel cycles in a shallow, productive, sub-arctic lake in interior Alaska, USA. Rates of CR varied 17-fold, strongly coupled to diel oscillations in water temperature. A weak inverse relationship to ~ 3 mg L−1 diel changes in dissolved organic carbon concentrations suggests CR partially modulated the standing stock of organic matter over short timescales. Average rates of CR were ~ 6 to 100-fold greater than published, conventional CR measurements, but comparable to existing free-water estimates of ecosystem respiration for nearby Alaskan lakes. Overall, this study places new weight on the importance of CR in whole-ecosystem biogeochemical transformations by supporting recent suggestions that planktonic CR may be commonly underestimated.

Keywords

Respiration Plankton Metabolism Community Food web Lake Diel 

Notes

Acknowledgements

We thank Jim Webster (Webster’s Flying Service) for transport to and from Canvasback Lake. This project was supported by funding provided to MJB from the Fonds de recherche du Québec–Nature et technologies (FRQNT) and the U.S. Permafrost Association (USPA); to RGS, DEB, and RGMS from National Aeronautics and Space Agency, NASA-ABoVE Project 14-14TE-0012 (awards NNH16AC03I and NNX15AU14A); to DEB from the University of Washington and the U.S. Geological Survey Land Resources Mission Area; and to RGS and MMD from the U.S. Geological Survey Land Resources and Water Mission Areas. We also thank two anonymous reviewers for providing helpful suggestions that improved our manuscript.

Supplementary material

27_2019_657_MOESM1_ESM.docx (427 kb)
Supplementary material 1 (DOCX 426 kb)

References

  1. Apple JK, del Giorgio PA, Kemp WM (2006) Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary. Aquat Microb Ecol 43:243–254CrossRefGoogle Scholar
  2. Badger MR, Von Caemmerer S, Ruuska S et al (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philos Trans R Soc B Biol Sci 355:1433–1446.  https://doi.org/10.1098/rstb.2000.0704 CrossRefGoogle Scholar
  3. Bogard MJ, Vachon D, St.-Gelais NF, del Giorgio PA (2017) Using oxygen stable isotopes to quantify ecosystem metabolism in northern lakes. Biogeochemistry 133:347–364.  https://doi.org/10.1007/s10533-017-0338-5 CrossRefGoogle Scholar
  4. Bogard MJ, Kuhn CD, Ellen Johnston S et al (2019) Negligible cycling of terrestrial carbon in many lakes of the arid circumpolar landscape. Nat Geosci 5:10.  https://doi.org/10.1038/s41561-019-0299-5 CrossRefGoogle Scholar
  5. Bushaw KL, Zepp RG, Tarr MA et al (1996) Photochemical release of biologically available nitrogen from aquatic dissolved organic matter. Nature 381:404–407CrossRefGoogle Scholar
  6. Cory RM, Ward CP, Crump BC, Kling GW (2014) Sunlight controls water column processing of carbon in arctic fresh waters. Science 345:925–928.  https://doi.org/10.1126/science.1253119 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cross WF, Hood JM, Benstead JP et al (2015) Interactions between temperature and nutrients across levels of ecological organization. Glob Chang Biol 21:1025–1040.  https://doi.org/10.1111/gcb.12809 CrossRefPubMedGoogle Scholar
  8. del Giorgio P, Williams P (2005) The global significance of respiration in aquatic ecosystems: from single cells to the biosphere. In: del Giorgio PA, Williams P (eds) Respiration in aquatic ecosystems. Oxford University Press, New York, pp 267–303CrossRefGoogle Scholar
  9. del Giorgio PA, Cole JJ, Cimbleris A (1997) Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385:148–151CrossRefGoogle Scholar
  10. Forget M-H, Carignan R, Hudon C (2009) Influence of diel cycles of respiration, chlorophyll, and photosynthetic parameters on the summer metabolic balance of temperate lakes and rivers. Can J Fish Aquat Sci 66:1048–1058.  https://doi.org/10.1139/F09-058 CrossRefGoogle Scholar
  11. Guillemette F, McCallister SL, del Giorgio PA (2013) Differentiating the degradation dynamics of algal and terrestrial carbon within complex natural dissolved organic carbon in temperate lakes. J Geophys Res Biogeosci 118:963–973.  https://doi.org/10.1002/jgrg.20077 CrossRefGoogle Scholar
  12. Hanson PC, Carpenter SR, Armstrong DE et al (2006) Lake dissolved inorganic carbon and dissolved oxygen: changing drivers from days to decades. Ecol Monogr 76:343–363CrossRefGoogle Scholar
  13. Harrell FE (2017) Package Hmisc: a package of miscellaneous R functions. Version 4Google Scholar
  14. Heglund PJ, Jones JR (2003) Limnology of shallow lakes in the Yukon Flats National Wildlife Refuge, interior Alaska. Lake Reserv Manag 19:133–140.  https://doi.org/10.1080/07438140309354079 CrossRefGoogle Scholar
  15. Hotchkiss ER, Hall RO (2015) Whole-stream 13C tracer addition reveals distinct fates of newly fixed carbon. Ecology 96:403–416.  https://doi.org/10.1890/14-0631.1 CrossRefPubMedGoogle Scholar
  16. Karl DM, Laws EA, Morris P et al (2003) Metabolic balance of the open sea. Nature 426:32.  https://doi.org/10.1038/426032a CrossRefPubMedGoogle Scholar
  17. Lauster GH, Hanson PC, Kratz TK (2006) Gross primary production and respiration differences among littoral and pelagic habitats in northern Wisconsin lakes. Can J Fish Aquat Sci 63:1130–1141.  https://doi.org/10.1139/f06-018 CrossRefGoogle Scholar
  18. Lewitus AJ, Kana TM (1995) Light respiration in six estuarine phytoplankton species: contrasts under photoautotrophic and mixotrophic growth conditions. J Phycol 761:754–761CrossRefGoogle Scholar
  19. Luz B, Barkan E, Sagi Y, Yacobi YZ (2002) Evaluation of community respiratory mechanisms with oxygen isotopes: a case study in Lake Kinneret. Limnol Oceanogr 47:33–42CrossRefGoogle Scholar
  20. Mopper K, Kieber DJ, Stubbins A (2014) Marine photochemistry of organic matter: processes and impacts. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter, 2nd edn. Academic Press, Cambridge, pp 389–450Google Scholar
  21. Pace ML, Prairie YT (2005) Respiration in lakes. In: del Giorgio PA, Williams PJL (eds) Respiration in aquatic ecosystems. Oxford University Press, New York, pp 103–121CrossRefGoogle Scholar
  22. Pollard PC (2013) In situ rapid measures of total respiration rate capture the super labile DOC bacterial substrates of freshwater. Limnol Oceanogr Methods 11:584–593.  https://doi.org/10.4319/lom.2013.11.584 CrossRefGoogle Scholar
  23. R development core team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  24. Read JS, Hamilton DP, Desai AR et al (2012) Lake-size dependency of wind shear and convection as controls on gas exchange. Geophys Res Lett 39:L09405.  https://doi.org/10.1029/2012GL051886 CrossRefGoogle Scholar
  25. Rusak JA, Tanentzap AJ, Klug JL et al (2018) Wind and trophic status explain within and among-lake variability of algal biomass. Limnol Oceanogr Lett 3:409–418.  https://doi.org/10.1002/lol2.10093 CrossRefGoogle Scholar
  26. Sadro S, Nelson CE, Melacka JM (2011) Linking diel patterns in community respiration to bacterioplankton in an oligotrophic high-elevation lake. Limnol Oceanogr 56:540–550.  https://doi.org/10.4319/lo.2011.56.2.0540 CrossRefGoogle Scholar
  27. Sadro S, Holtgrieve GW, Solomon CT, Koch GR (2014) Widespread variability in overnight patterns of ecosystem respiration linked to gradients in dissolved organic matter, residence time, and productivity in a global set of lakes. Limnol Oceanogr 59:1666–1678.  https://doi.org/10.4319/lo.2014.59.5.1666 CrossRefGoogle Scholar
  28. Schindler DE, Jankowski K, A’Mar ZT, Holtgrieve GW (2017) Two-stage metabolism inferred from diel oxygen dynamics in aquatic ecosystems. Ecosphere 8:e01867.  https://doi.org/10.1002/ecs2.1867 CrossRefGoogle Scholar
  29. Spencer RGM, Pellerin BA, Bergamaschi BA et al (2007) Diurnal variability in riverine dissolved organic matter composition determined by in situ optical measurement in the San Joaquin River (California, USA). Hydrol Process 21:3181–3189.  https://doi.org/10.1002/hyp.6887 CrossRefGoogle Scholar
  30. Staehr PA, Baastrup-Spohr L, Sand-Jensen K, Stedmon C (2012a) Lake metabolism scales with lake morphometry and catchment conditions. Aquat Sci 74:155–169.  https://doi.org/10.1007/s00027-011-0207-6 CrossRefGoogle Scholar
  31. Staehr PA, Testa JM, Kemp WM et al (2012b) The metabolism of aquatic ecosystems: history, applications, and future challenges. Aquat Sci 74:15–29.  https://doi.org/10.1007/s00027-011-0199-2 CrossRefGoogle Scholar
  32. Szyper JP, Rosenfeld JZ, Piedrahita RH, Giovannini P (1992) Diel cycles of planktonic respiration rates in briefly incubated water samples from a fertile earthen pond. Limnol Oceanogr 37:1193–1201.  https://doi.org/10.4319/lo.1992.37.6.1193 CrossRefGoogle Scholar
  33. Taylor CD, Doherty KW (1990) Submersible incubation device (SID), autonomous instrumentation for the in situ measurement of primary production and other microbial rate processes. Deep Sea Res Part A Oceanogr Res Pap 37:343–358.  https://doi.org/10.1016/0198-0149(90)90132-F CrossRefGoogle Scholar
  34. Thomas MK, Fontana S, Reyes M et al (2018) The predictability of a lake phytoplankton community, over time-scales of hours to years. Ecol Lett 21:619–628.  https://doi.org/10.1111/ele.12927 CrossRefPubMedGoogle Scholar
  35. Vachon D, Prairie YT, Guillemette F, del Giorgio PA (2017) Modeling allochthonous dissolved organic carbon mineralization under variable hydrologic regimes in boreal lakes. Ecosystems 20:781–795.  https://doi.org/10.1007/s10021-016-0057-0 CrossRefGoogle Scholar
  36. Vorobev A, Sharma S, Yu M et al (2018) Identifying labile DOM components in a coastal ocean through depleted bacterial transcripts and chemical signals. Environ Microbiol 20:3012–3030.  https://doi.org/10.1111/1462-2920.14344 CrossRefPubMedGoogle Scholar
  37. Weger HG, Herzig R, Falkowski PG, Turpin DH (1989) Respiratory losses in the light in a marine diatom: measurements by short-term mass spectrometry. Limnol Oceanogr 34:1153–1161.  https://doi.org/10.4319/lo.1989.34.7.1153 CrossRefGoogle Scholar
  38. Williams PJLB, Morris PJ, Karl DM (2004) Net community production and metabolic balance at the oligotrophic ocean site, station ALOHA. Deep Res Part I Oceanogr Res Pap 51:1563–1578.  https://doi.org/10.1016/j.dsr.2004.07.001 CrossRefGoogle Scholar
  39. Woolway RI, Jones ID, Maberly SC et al (2016) Diel surface temperature range scales with lake size. PLoS One 11:e0152466.  https://doi.org/10.1371/journal.pone.0152466 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Yvon-durocher G, Allen AP, Montoya JM et al (2010) The temperature dependence of the carbon cycle in aquatic ecosystems. In: Woodward G (ed) Advances in ecological research, vol 43. Academic, Burlington, pp 267–313Google Scholar
  41. Yvon-Durocher G, Caffrey JM, Cescatti A et al (2012) Reconciling the temperature dependence of respiration across timescales and ecosystem types. Nature 487:472–476.  https://doi.org/10.1038/nature11205 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.School of Environmental and Forest SciencesUniversity of WashingtonSeattleUSA
  2. 2.Florida State UniversityTallahasseeUSA
  3. 3.United States Geological SurveyBoulderUSA
  4. 4.School of Engineering and Environmental SciencesUniversity of WashingtonSeattleUSA
  5. 5.Department of Biological SciencesUniversity of LethbridgeLethbridgeCanada

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